Biosonar, dive, and foraging activity of satellite tracked ...mmtcorp.co.jp/A-tag/papers/Linnenschmidt2012.pdf · Satellite Tag A satellite transmitter (SPOT5, Wildlife Computers,

MARINE MAMMAL SCIENCE, 29(2): E77–E97 (April 2013)© 2012 by the Society for Marine MammalogyDOI: 10.1111/j.1748-7692.2012.00592.x

Biosonar, dive, and foraging activity of satellite trackedharbor porpoises (Phocoena phocoena)

MEIKE LINNENSCHMIDT,1 Institute of Biology, University of Southern Denmark,Campusvej 55, DK-5230, Odense M, Denmark; JONAS TEILMANN, Department ofBioscience, Aarhus University, Frederiksborgvej 399, DK-4000, Roskilde, Denmark;

TOMONARI AKAMATSU, National Research Institute of Fisheries Engineering, 7620-7,Hasaki, Kamisu, Ibaraki, 314-0408, Japan and Japan Science and Technology Agency,

CREST, Sanbancho, Chiyoda-ku, Tokyo, 102-0075, Japan; RUNE DIETZ, Department ofBioscience, Aarhus University, Frederiksborgvej 399, DK-4000, Roskilde, Denmark; LEEA. MILLER, Institute of Biology, University of Southern Denmark, Campusvej 55, DK-5230, Odense M, Denmark.

Abstract

This study presents bioacoustic recordings in combination with movementsand diving behavior of three free-ranging harbor porpoises (a female and twomales) in Danish waters. Each porpoise was equipped with an acoustic data log-ger (A-tag), a time-depth-recorder, a VHF radio transmitter, and a satellitetransmitter. The units were programmed to release after 24 or 72 h. Possibleforaging occurred mostly near the surface or at the bottom of a dive. Theporpoises showed individual diversity in biosonar activity (50,000clicks per hour) and in dive frequency (6–179 dives per hour). We confirm thatwild harbor porpoises use more intense clicks than captive animals. A positivetendency between number of dives and clicks per hour was found for a subadultmale, which stayed near shore. It showed a distinct day-night cycle with lowecholocation rates during the day, but five times higher rates and higher diveactivity at night. A female traveling in open waters showed no diel rhythm,but its sonar activity was three times higher compared to the males’. Consider-able individual differences in dive and echolocation activity could have beeninfluenced by biological and physical factors, but also show behavioral adapt-ability necessary for survival in a complex coastal environment.

Key words: acoustic tag, TDR, biosonar, echolocation, diving, foraging, harborporpoise, Phocoena phocoena, Danish waters, Kattegat, Great Belt, Argos.

Most of our knowledge concerning echolocation and acoustic communicationstems from studies of harbor porpoises in captivity (Møhl and Andersen 1973;Kastelein et al. 1995; Goodson and Sturtivant 1996; Au et al. 1999; Teilmannet al. 2002; Verfuß et al. 2005, 2009; Atém et al. 2009; DeRuiter et al. 2009;Clausen et al. 2010; Miller 2010). However, there is one full bandwidth

1Corresponding author (e-mail: [email protected]).

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recording of echolocation by free ranging harbor porpoises where Villadsgaardet al. (2007) documented that animals in the wild use more intense clicks (178–205 dB re 1 lPa peak-to-peak) than those in captivity (129–174 dB re 1 lPapeak-to-peak, Linnenschmidt et al. 2012). There are also studies using stationaryacoustic data loggers (like T-PODs) for long term monitoring of harborporpoises (Carstensen et al. 2006). While such field studies document the pres-ence and sonar signal characteristics of wild porpoises, they reveal little aboutthe behavior of individual animals in their natural environment.Gill net fishing is a major threat to harbor porpoises (e.g., Vinther and Larsen

2004). Acoustic alarms (pingers) on fishing gear effectively reduce bycatchduring experiments in commercial fisheries (Kastelein et al. 2001, Carlströmet al. 2002). However, concern has been raised that extensive use of pingers mayresult in habitat exclusion. Gill nets with higher acoustic detectability wouldhopefully be the better choice to reduce bycatch in general (Teilmann et al.2006). However, we lack detailed understanding about the natural bioacousticsand diving behavior of harbor porpoises and under which circumstances they arebycaught in nets. Such knowledge gathered from free ranging animals wouldimprove mitigation of harbor porpoise bycatch.For nearly 10 yr acoustic tags have been deployed on individual whales

(e.g., Madsen et al. 2002; Johnson et al. 2004, 2009; Akamatsu et al. 2005a, b;Goldbogen et al. 2006; Oleson et al. 2007). There are basically three types ofacoustic tags; Bprobes (Acousonde), D-tags and A-tags. The Acousonderecords dive and acoustic behavior. It has recently been deployed on pantropicalspotted dolphins and short-finned pilot whales (http://www.acousonde.com).Due to the maximum recording frequency of 100 kHz it is inappropriate forrecording the high frequency (120–140 kHz) echolocation and communicationclicks of harbor porpoises. Its predecessor, the Bprobe, has been deployed on finwhales (Goldbogen et al. 2006) and blue whales (Oleson et al. 2007), amongothers. The D-tag provides short-term, but highly detailed information on theacoustic environment, the swimming and diving behavior and the acousticperformance of the host animal (Johnson and Tyack 2003). It records acousticsignals up to 96 kHz (Arranz et al. 2011). At its present stage it is deployedwith suction cups that do not allow for observations over consecutive days.D-tags have been attached to several species of larger whales (Miller et al.2004; Johnson et al. 2004, 2009, Shapiro 2006; Aguilar Soto et al. 2008;Arranz et al. 2011). The A-tag functions as an event recorder of short clicks upto more than 200 kHz and it registers time of occurrence, the amplitude andthe bearing of signals within a defined bandwidth (Akamatsu et al. 2005a).The A-tag has been deployed on finless porpoises (Neophocaena phocaenoides)(Akamatsu et al. 2005b, 2010) and white-beaked dolphins (Lagenorhynchusalbirostris).2 In a pilot study the A-tag has been deployed on a harbor porpoisein Danish waters and recorded acoustic activity for 4.5 h (Akamatsu et al.2007). The results showed the potential use of the A-tag combined with asatellite transmitter for studying the bioacoustics, dive behavior and movementsof wild harbor porpoises.

2Rasmussen, M. H., T. Akamatsu, J. Teilmann, G. A. Vikingsson and L. A. Miller. 2011. Bioso-nar, diving and movements of two tagged white-beaked dolphin in Icelandic waters. Deep-SeaResearch II. (accepted for publication).

E78 MARINE MAMMAL SCIENCE, VOL. 29, NO. 2, 2013

Here we present recordings over several days (22–67 h) of acoustic activity,dive profiles and movements of three free ranging harbor porpoises, eachequipped with an A-tag, a dive recorder and a satellite transmitter.

Methods

Study Area, Subjects, and Capture Method

In April 2006 and May 2007 three harbor porpoises, an adult male (#1),a subadult male (#2), and an adult female (#3) were captured in the Kattegatand Great Belt (Fig. 1) using pound nets (see Teilmann et al. 2007). The por-poises were tagged with several instruments and data collected for 23:40 h,63:35 h, and 67:51 h, respectively.

Figure 1. Satellite tracking map for the three porpoises in the present study. The areashown is the Inner Danish waters located between the mainland of Denmark (Jutland) tothe west and southern Sweden to the east. Colored lines represent the movements of theanimals during the tagging period. Yellow: porpoise #1. Green: porpoise #2. Red:porpoise #3. The colored dots represent locations for each day; yellow the day of tagging,black the second day (last day for #1), green the third day and purple the last (forth) dayfor #2 and #3. The blue stars show the position of tagging and the yellow stars showwhere the tags were released. (See Table 1 for information on the tagged animals).

LINNENSCHMIDT ET AL.: TAGGED WILD HARBOR PORPOISE BIOSONAR E79

The water depth in the study area is mostly less than 50 m except in thenortheast where deeper waters occur. Water temperatures vary throughout theyear between about 0°C and +20°C. The physical parameters of the region aredominated by an inflow of saline water from the North Sea and an outflow ofestuarine water from the Baltic Sea making the Kattegat and Great Belt acomplex oceanographic system (see Rheinheimer 1996 for details).

Acoustic Data Logger and VHF Transmitter

The porpoises were equipped with an A-tag W20-AS (stereo hydrophone,Little Leonardo, Tokyo, Japan, Fig. 2A). The tag functions like an ultrasonicevent recorder and records the sound pressure along with the exact time ofdetection at each hydrophone (clock drift: 1 s/d). Signals were band pass filtered(55–235 kHz) and a hardware detection threshold was set at 142 dB (peak-to-peak re 1 lPa). The sampling frequency of 2 kHz for W20-AS provided a timeresolution and shortest click interval of 0.5 ms. The total recording time isbattery limited to 60–70 h. All components fit into a cylindrical waterproofhousing measuring 21 9 122 mm weighing 77 g.The A-tag was imbedded in a float (Fig. 2D) for positive buoyancy after the

detachment. Also embedded into the float was a VHF transmitter (MM130,ATS, Isanti, MN) for locating the data logging tags (Fig. 2E). Detailed informa-tion on the A-tag is available in Akamatsu et al. (2005a).

Figure 2. Dorsal fin of a harbor porpoise showing the tags: (A) stereo-acoustic A-tag,(B) time-depth recorder, (C) release devise and cable tie, (D) float with data logging tags,(E) VHF radio transmitter, (F) aluminum backing plate with protecting closed cell neo-prene (G), (H) satellite tag.


Diving Recorder

A time and depth recorder (DST-milli; Star-Oddi, Reykjavik, Iceland) wasattached to the float (Fig. 2B). According to the manufacturers specifications, thedata resolution and accuracy of the depth recorder is 0.03% (12 bits) of full scale(900 m, i.e., ±27 cm) and ±0.4% of depth reading, respectively. Both limit theminimum resolution of the data. The sampling rate for the three porpoises was cho-sen to be 1, 4, and 3 s for porpoises #1, #2, and #3, respectively. A dive was definedwhen the porpoise was below 2 m for at least 6 s.

Satellite Tag

A satellite transmitter (SPOT5, Wildlife Computers, Redmond, WA) with anoval shape measuring 10 9 3.5 9 1 cm was attached to the dorsal fin oppositethe acoustic package (Fig. 2H). The satellite transmitter was set to transmitevery 45 s when at the surface. When the preset maximum (250 transmis-sions (equals 4–7 h/d) for the first two animals or 1,000 transmissions (equals22–24 h/d) for the third animal) was reached no further positions were availablefor that day. Satellite positions were obtained from the ARGOS satellite systemand had an accuracy of less than 100 m to a few kilometers. We used thesatellite positions to link acoustic and dive behavior with the habitat as well astracking the long-term movements after the acoustic package was detached.

Tagging Procedure

Captive animals were slowly brought into reach by raising the pound net to thesurface, carefully lifting the animal on board, and placing it on a soft pad on thedeck of our boat. Only sub adult or adult animals without injuries and in good con-dition were selected for tagging. The satellite tag was mounted to the left side ofthe dorsal fin with two 5 mm silicone covered Delrin pins while the data loggingtags and a release mechanism was placed on the right side. The hydrophones on theA-tag were 40–50 cm behind the blowhole (Fig. 2). During the tagging procedure(~30 min) the heart and respiration rates were continuously monitored. The floatwith the data logging tags, consisting of the A-tag, time-depth recorder, and VHFtransmitter, (Fig. 2) was positively buoyant in water. The satellite-tag remained onthe porpoise until the iron nuts corroded after about 1 yr. For more details on thetagging procedure and condition of the animals see Teilmann et al. (2007), Eskesenet al. (2009), and Sonne et al. (2012).

Release and Recovery of the Tag

The release mechanism consisted of a plastic strip with a timer and a smalldetonator (Little Leonardo, Tokyo, Japan) connected to an aluminum back platewith a hook that kept the float with the data logging tags in place (Fig. 2C).The timer was programmed to release the float after 24 h, 72 h, and 72 h forporpoise #1, #2, and #3, respectively.An ARGOS position of the animal at the time of detachment helped to locate

the search area to within a radius of a few kilometers. A directional three or fiveelement Yagi antenna and a VHF receiver (ICOM R10) were used to locate theVHF radio signal from the float with the data logging tags.


Data Analysis

Data collected by the A-tag were processed in custom-made software in IGORPro 5 (WaveMetrics, Portland, OR). Two temporal filters were used before themajority of recordings were analyzed. First, splash noise from the animal breakingthe surface was excluded by deleting data from 0 to 30 cm below the surface. Thesecond filter reduced surface echoes that typically occurred at delays of about 0.5–2.5 ms after reception of the direct signal. In the following text we refer to detec-tions as all acoustic triggerings of an A-tag before filtering. We refer to clicks as alldetections after the data set has been filtered with the two temporal filters. How-ever, no temporal filters were used when analyzing possible foraging sequences.Owing to copious data and for comparing to previous studies, our results

(clicks and dives) were pooled in 1 h time bins. Dives were manually countedand attributed to the time bin in which it started. Maximum dive depth wasmeasured for each dive and averaged into 1 h time bins.We used three criteria to define a possible foraging event. A click train had to

include three parts: search, approach (initial and terminal part), and an indicationof the buzz (see Fig. 7) to be defined as a possible prey capture sequence. Inaddition the click interval at the end of the approach had to be below 10 ms.These criteria were defined based on results of prey capture events by captiveharbor porpoises in the facility at Fjord&Bælt, Kerteminde, Denmark (Atémet al. 2009, Verfuß et al. 2009). The levels of clicks recorded at the dorsal fin are30 to 40 dB lower than the source level (1 m in front of the animal on theacoustic axis) (Hansen 2005). These attenuations have recently been verified withdirect measurements using an A-tag attached with suction cups on a captive har-bor porpoise approaching and echolocating on a hydrophone as a target atFjord&Bælt (LAM, unpublished data). Since the threshold of the A-tag was142 dB (peak-to-peak) re 1lPa, low amplitude clicks were not recorded, espe-cially those during the buzz just before and during prey capture (see Fig. 7 andMiller 2010). Thus the actual number of clicks produced by the animals and themaximum click rates are underestimated in this study.We used parametric and nonparametric statistical tests according to Fowler

et al. (1998) using Microsoft Office Excel 2007.

Results

There was considerable individual variation in biosonar, diving activity, anddistance covered among the tagged animals. Porpoises #2 and #3 were tagged inHevring Bight while porpoise #1 was tagged in the Great Belt (Fig. 1 andTable 1). Porpoise #1 swam off shore about 67 km while it carried the data log-ging tags. Porpoise #2 swam about 70 km with the tags attached and stayednear the coast for the full recording time (Fig. 1). Porpoise #3 spent most of itstime in the open waters of the Kattegat and swam about 200 km with the datalogging tags. We registered about four times the number of clicks per hour(24,227) for porpoise #3 compared to the other two porpoises (6,506 and 6,546;Table 1). Not surprisingly, the two porpoises in open waters (#1 and #3) dovedeeper than the porpoise near the coast (#2). Periods without detection of clickswere evident for all tagged porpoises (Table 1). The coastal porpoise (#2) hadthe longest maximum period without click detections (1,300 s), while porpoise


#1 and #2 had maximum periods without click detections of 236 s and 99 s,respectively. See Table 1 for more statistics.

Temporal Changes in Biosonar Activity

Porpoise #1 swam in the Great Baelt (Fig. 1). The biosonar activity of thisporpoise increased from 3,000 clicks to over 12,500 per hour during the daytimeand peaked to more than 19,000 clicks per hour around midnight. Hereafter theclick activity dropped gradually to near zero during the morning hours beforethe float with the data logging tags was released (Fig. 3).

Table 1. Data for three tagged harbor porpoises in the Kattegat and Great Belt. Posi-tions separated by less than half an hour were deleted for distance and swimming speedcalculations (See also Fig. 1), n gives the number of full hours of analyzed data.

Harbor porpoise ID200606422(2006 #1)

200606172(2006 #2)

200706170(2007 #3)

Location Great Belt Hevring Bight Hevring BightLongitude, latitude 55.5ºN, 11ºE 56.5ºN, 10.5ºE 56.5ºN, 10.5ºESex M M FAge group Adult Subadult AdultStandard length (cm) 149 111 166Weight (kg) 53 - 62Date and time of tagging 23 April 2006,

111026 April 2006,1620

19 May 2007,1240

A-tag type W20-AS W20-AS W20-ASTotal attachment time (h:m) 23:40 63:35 67:51Duration of satellite tracking(d)

202 201 27

Min. distance swam withfloat (km)

67 73 203

Min. average swim speed(km/h)

8.0 2.6 4.0

Total number of dives 906 2,659 2,815Average number of dives perhour

41 (n = 23,SD = 14)

44 (n = 60,SD = 17)

47 (n = 60,SD = 45)

Average dives/hour duringday

48 (n = 13,SD = 10)

33 (n = 31,SD = 9)

49 (n = 34,SD = 55)

Average dives/hour duringnight

32 (n = 10,SD = 14)

56 (n = 29,SD = 15)

44 (n = 26,SD = 27)

Max. dive duration (s) 94 138 213Max. dive depth (m) 25 14 34Total number of detections 467,380 622,467 2,831,044Total number of clicksa 144,018 390,331 1,623,240Average clicks/hour 6,546 (n = 22) 6,506 (n = 60) 24,227 (n = 67)Average clicks/hour duringday

5,370 (n = 12) 2,412 (n = 31) 23,625 (n = 36)

Average clicks/hour duringnight

7,958 (n = 10) 10,882 (n = 29) 24,927 (n = 31)

Max. period without anyclicks (s)

236 1,300 99

aResidual detections (clicks) after noise filtering.


Porpoise #2 swam in coastal waters and showed clear diurnal patterns ofbiosonar activity (two-tailed t-test, P < 0.0001) whereas porpoise #3 swam offshore in the Kattegat, and did not show such tendencies (Fig. 3). The biosonaractivity of porpoise #2 was below 3,000 clicks per hour during the afternoonafter tagging (Fig. 3). During the evening and early night the rate of clicks perhour increased gradually and peaked during the second part of the night withmore than 16,000 registered clicks per hour. After two hours with intenseecholocation a sharp decline in the clicking rate occurred from early morningand for the following 14 h (

Porpoise #2 dove more at night than during the day (two-tailed t-test,P < 0.0001). It remained in coastal waters for the entire tagging period (Fig. 1).Hence the dive depths were shallow, between 4 and 11 m on average (Fig. 5).We recorded lower dive frequencies (minimum 21 dives per hour) around noonand the highest dive activity at midnight with more than 50 dives per hour.Dive activity decreased towards dawn. The same pattern occurred during allthree nights for porpoise #2 (Fig. 4). There was a positive correlation betweendive and acoustic activity for this porpoise (Fig. 6A, r2 = 0.66, P < 0.0001).

Figure 4. Changes in dive rates with time. The figure shows the number of dives in1 h time bins for the three tagged harbor porpoises. A dive was tallied in the time binin which it started. A dive was defined as having at least one data point below 2 m andlasting a minimum 6 s. Shading shows night-time hours with dusk starting at 2000and dawn at 0600. Note that porpoise #2 shows a tendency for more dives at night thanduring the day (see Fig. 3 for click rates).


Porpoise #3 had high dive activity (>160 dives per hour) for several hoursafter tagging (Fig. 4). After a short decrease in dive activity during the earlyevening her dive rate increased to between 60 and 120 dives per hour during thefirst night. Throughout the rest of the tag deployment the dive frequency stayed

Figure 6. Relation between dive frequency and recorded clicks per hour for the three ani-mals. The graph on the left for porpoise #2 shows a modest positive correlation betweendive frequency and biosonar activity. This trend is not seen for porpoise #1 or #3.

Figure 5. Average maximum dive depth in 1 h time bins during the time the threeharbor porpoises carried the acoustic and dive tags. A dive was tallied in the hour in which itstarted. The red symbols represent possible foraging activity within that particular hour.Shading shows night-time hours with dusk starting at 2000 and dawn at 0600. See Table 1for tagging dates and times and Figure 7 for illustrations of possible foraging events.


around 30 dives per hour. The dive frequency and the biosonar activity showedno correlation (Fig. 3, 4, 6). Porpoise #3 had the greatest variation in averagedive depth per hour. During the first day and night it did not dive deeper than8 m on average (Fig. 5). As porpoise #3 moved into deeper waters of theKattegat (Fig. 1), its average dive depth per hour increased gradually to a maxi-mum of 24 m during day 3 (Fig. 5). There was no obvious correlation betweendiving and acoustic activity for porpoise #3 (Fig. 6B).

Possible Prey Capture Events

An example of possible foraging behavior from two of the tagged animals isshown in Figure 7. No temporal filtering was performed on the recordings of

Figure 7. Possible foraging events from two free ranging harbor porpoises with acous-tic tags. A is from porpoise #1 feeding near the surface (0–2 m) and B is from porpoise#3 feeding near or at the sea bottom (see also Fig. 5). Click trains are shown with arbi-trary phases of search, approach, and buzz based on prey capture by captive harbor por-poises. The buzz is not resolved here. Also shown is a possible point of prey detection(circle in A) and possible points of prey captures (boxes). Surface and bottom echoes haveclick intervals on the order of 0.5 ms and are seen as horizontal lines of dots. No tempo-ral filters were used here. Note that in B, estimated on axis source levels can be as highas 190 to 200 dB re 1 lPa peak-to-peak (see the Results and Discussion). Note also thedifferent time axes and that the possible prey capture event occurs faster in B than in A.


possible foraging behavior. We illustrate one possible feeding event where porpoise#2 was within the surface layer (0–2 m depth) (Fig. 7A) and porpoise #3 was atthe bottom of its dive, and may have been at or near the sea bottom (Fig. 7B). Thechanges in the click interval patterns were similar to those described by Verfußet al. (2009) from the captive animals at Fjord&Bælt, and we therefore adoptedtheir terminology. Three phases can be seen in Figure 7; search as well as initialand terminal parts of the approach. During the search phase click intervals variedbetween 30 and 150 ms. The initial part of the approach began with the possiblepoint of prey detection and lasted for 0.5 s. During this time click intervalsdecreased rapidly from approximately 80 ms to 10 ms. The A-tag captured only afew clicks of the terminal part of the approach where the click intervals were below10 ms and constantly decreasing to a minimum click interval of 3 ms. The termi-nal part presumably ended with a buzz (not recorded) and a possible prey capture(Fig. 7). Echoes reflecting from the surface and the bottom had intervals of about0.5 ms (Fig. 7). The clicks of both animals varied in intensity from about 144 dBto about 163 dB re 1 lPa peak-to-peak (20 to 160 Pa) recorded by the A-tag nearthe dorsal fin, or 30 to 40 dB greater for source levels (Fig. 7).Click trains that showed consecutive patterns of possible feeding events were

tallied individually (Table 2). Porpoises #1 and #3 had the greatest number ofpossible feeding events near the surface (0–2 m depth). Porpoise #3 also foragedat the bottom of its dives, as did the other porpoises, except they showed fewerpossible foraging events. Porpoise #1 showed most of its presumed foraging dur-ing the late afternoon and night while porpoise #2 showed almost all presumedforaging events during the night. Porpoise #3 had possible foraging events dur-ing the day and night (Fig. 5).Figure 8 summarizes the occurrence of possible foraging, diving and biosonar

activity on a 24 h cycle. Porpoise #1 had high foraging activity during the firstpart of the recording with 61 possible feeding events mostly in the afternoonand early evening hours. We found no foraging behavior during the second partof the recording for porpoise #1. Porpoise #2 showed only two possible feedingevents during the day and 11 at night (Fig. 5, 8). Porpoise #3, however, showedforaging throughout the full recording time and we identified a total of 161possible feeding events.

Discussion

To our knowledge these are the longest acoustic recordings from free-rangingcetaceans. In addition this is the first time geographical locations are associated

Table 2. Number of possible foraging events and where these occurred during eachdive phase for each animal. Short click intervals indicating approach to the sea bottom orthe surface were discarded in the analyses (see Methods). Porpoises #1 and #3 were swim-ming mostly in deeper waters while porpoise #2 stayed in shallow water with sandbottom near the coast (see Fig. 1).

Porpoise Foraging events Surface Descending Bottom Ascending

#1 61 46 2 2 11#2 13 3 0 7 3#3 161 115 1 42 3


Figure8.

Summaryof

dive,

biosonar

andpossible

foragingactivity

fora24hcycletalliedin

1htimebins.Notedifferencesin

theordinate

axes.Shadingshow

snighttim

ehours

withdusk

startingat

2000anddaw

nat

0600.


with acoustic activity. The three tagged harbor porpoises utilized three differenthabitats; the Great Belt (#1), the coastal Kattegat (#2) and the central part ofthe Kattegat (#3) (see Fig. 1). Thus, it is not surprising that the porpoisesexhibited different diving and biosonar behaviors even though all instrumentshad the same specifications and adjustments.The A-tag had a threshold level of 142 dB re 1 lPa (peak-to-peak), which is

not sensitive enough to register all of the animal’s echolocation signals. The elec-tronic noise floor prohibits lower thresholds (Akamatsu et al. 2005a). However,the animal’s own signal recorded at the dorsal fin is attenuated by 30–40 dBrelative to the source level recorded 1 m in front of the animal. Villadsgaardet al. (2007) reported source levels of wild harbor porpoises in Danish watersranging between 178 and 205 dB re 1 lPa peak-to-peak, and our A-tag record-ings confirm these values (see Fig. 7). This means that the minimum source levelat the dorsal fin of a tagged wild harbor porpoise would be about 148–175 dBre 1 lPa, which is greater than the threshold level of the A-tag (142 dB re 1lPa). We therefore believe that most echolocation signals from our taggedporpoises were recorded. However, during the buzz the source levels are low andthe repetition rate is very high, about 500 clicks per second (Beedholm andMiller 2007, Atém et al. 2009, DeRuiter et al. 2009). Thus buzz clicks mostlikely did not trigger our system.The settings of the software temporal filters were chosen in order to avoid

detections caused by splash noise to a depth of 0.3 m and surface reflections withclick intervals shorter than 2.5 ms. Surface reflections with longer click intervalswere rarely recorded, probably due to the distance related transmission loss andthe rather high threshold of the A-tag. High rate detections not produced by aporpoise were sporadic and did not limit our analyses. Thus, we believe that thedifferences in biosonar activity among animals are real and not influenced by ourinstrumentation.Inevitably, all forms of tags may influence an animal’s behavior. However,

harbor porpoises can carry functional satellite tags for a year while moving overlong distances thus indicating that satellite tags alone are tolerated (Edrén et al.2010, Sveegaard et al. 2010). Also, two harbor porpoises carrying satellite tagswere bycaught in gillnets by fishermen. Both animals were in good nutritionalstatus and had full stomachs (Sonne et al. 2012), suggesting natural behavior ofsatellite tagged harbor porpoises. A captive harbor porpoise showed minorchanges in behavior immediately after tagging. The altered behaviors, whichwere likely due to valium sedation, continued for the next 7–24 h after whichthe behaviors returned to normal (Geertsen et al. 2004). Although no valiumsedation was used in the present study, the behavior of our animals could havebeen influenced by the tags and the tagging procedure.

Biosonar Activity

Although three tagged harbor porpoises is a small sample size, we found someinteresting differences in acoustic and dive behavior among the animals. Allanimals showed higher click activity during the night (Table 1), which wasexpected considering the advantage of biosonar for orientation and foragingduring darkness. If light availability should influence biosonar activity, then wewould expect captive harbor porpoises with blinding eyecups to alter their bioso-nar signals. However, there is no significant difference between click source


levels used by a captive harbor porpoise with and without blinding eyecups(t-test, P > 0.05; LAM, unpublished data). Also DeRuiter et al. (2009) found nodifferences in click phases, intervals and levels during prey capture for porpoiseswith or without eyecups. Therefore we assume that the day-night differences wereport here are influenced by something other than just illumination.Porpoises will change biosonar levels depending on circumstances. Porpoise #2

stayed entirely in shallow sandy-bottom waters near the coast (Fig. 1). Harborporpoises, and other odontocetes, decrease the source level of their biosonar withdecreasing distance to a target (Rasmussen et al. 2002, Au and Benoit-Bird2003, Beedholm and Miller 2007, Atém et al. 2009, DeRuiter et al. 2009).Hence, the shallow water depth does not demand intense, long-range echoloca-tion unless the animal was detecting fish while swimming horizontally. Alsoproximity to the bottom will increase clutter echoes that might cause the por-poise to further reduce the level of its clicks. Porpoise #2 had the longest periodwith no triggers on the A-tag (Table 1) indicating it used less intense clickswhile in shallow waters. Porpoises #1 and #3 spent some time in deeper water.Villadsgaard et al. (2007) recorded the highest source levels from animals in thedeepest waters. From the results presented here and from our experience withanimals in captivity, we conclude that harbor porpoises echolocate almost contin-uously, although diurnal variations and infrequent silent periods of severalminutes may occur. We thus conclude that the diurnal behavior in both echolo-cation and diving and the variability between animals is real and not an artifactof the technical limitations of the equipment. However it is important to notethat not all clicks the tagged porpoises emit are necessarily recorded because ofthe A-tag threshold.Porpoise #2, which stayed in the shallow sandy-bottom waters near the coast,

used more biosonar at night (Fig. 3) and had most feeding bouts at night(Fig. 5). We assume this individual was feeding on fish like juvenile flat fish(Pleuronectiformes) that are commonly found in the area according to fishermen.These fish show nocturnal activity and movements (Verheijen and De Groot1967) that could explain the diel biosonar activity by porpoise #2. Furthermore,this animal had higher diving activity at night (Table 1, Fig. 4) that correlatedwith higher biosonar activity (Fig. 3, 4, 6), both of which support our sugges-tion that porpoise #2 was taking nocturnal fish. Porpoises #1 and #3 foragedboth in daylight and darkness (Fig. 5). Thus, these two porpoises were probablyforaging on fish like sandeels (Ammodytes sp.) during the day (Winslade 1974)and at night on fish like herring, sprat (Sprattus sprattus), and flatfish that arenight active (Verheijen and De Groot 1967, Cardinale et al. 2003).The high biosonar activity of porpoise #3 is difficult to explain by foraging

activity alone in that porpoise #1 also foraged in offshore waters, but showed lowerbiosonar activity (Fig. 3). Perhaps porpoise #3, a larger female that used moreintense signals, had higher energetic requirements and thus more biosonar activityto find prey, or there were significant differences in prey type and availability inthe two areas. A combination of the above factors probably accounts for the greaternumber of registered clicks from porpoise #3 compared to the other two porpoises.

Diving Activity

The hourly mean dive frequencies of about 45 dives per hour (range 4–185)were similar for the three porpoises (Table 1). We define a dive as exceeding 6 s


at a depth below 2 m. In comparison 14 porpoises tagged in the same generalarea as our study had 29 dives per hour on average (range 1–53) during April toAugust with little variation between months (Teilmann et al. 2007). The differ-ences between earlier studies in the same general geographical area and this onemay reflect individual or habitat dependent variations. It might also be due tothe slightly different definition of a dive. Teilmann et al. (2007) defined a diveas lasting longer than 10 s at a depth below 2 m. The number of dives per hourrecorded for porpoises in the western Atlantic (Westgate et al. 1995) rangedfrom 12 to 109, which is similar to our study. Westgate et al. (1995) defined adive as lasting longer than 3 s at a depth below 2 m. The differences in mini-mum dive duration certainly affect the number of dives counted, especially inshallow waters where dive rates, according to the present study, tend to increasedrastically. Comparing the present study with the one by Teilmann et al. (2007),the greater minimum dive duration in their study probably excluded many divesand therefore revealed fewer high dive rates. The study by Westgate et al. (1995)was conducted in the Bay of Fundy, Canada, which has deeper waters than ourstudy area. However, Westgate et al. (1995) did not correlate the dive rates towater depth and, therefore, we cannot say if their highest recorded dive rate (109dives per hour), which occurred in shallow waters, was due to the affect of tag-ging or simply due to the variability of natural behavior among animals.Dive activity was equally distributed throughout the day, but one porpoise

(#2) showed a diel diving pattern with fewer and sometimes deeper dives dur-ing the day. The increased diving frequency at night could indicate a highereffort in finding night active juvenile flat fish as discussed above. Porpoises #1and #3 did not show such correlations or diel diving patterns, but rather theyhad constant dive frequencies throughout most of the recording time. However,porpoise #3 showed extremely high dive rhythms (up to 180 dives per hour)for six hours after tagging (Fig. 4). That its behavior was affected by the tag-ging procedure can therefore not be excluded. But according to observations atthe facility in Kerteminde, Denmark, dive frequencies of captive harbor por-poises in shallow waters of the enclosure can easily reach similar high valuesunder normal non-stressed conditions.3 All three porpoises were tagged inpound nets that are set in shallow waters. Two of the three animals showedhigh diving frequencies after tagging, but the third (#2) did not, so we cannotconclude that the tagging procedure alone was responsible for initial highdiving frequencies.

Possible prey capture

Trained harbor porpoises in simulated prey capture experiments (Atém et al.2009, DeRuiter et al. 2009, Verfuß et al. 2009, Miller 2010) show the samethree phases in their echolocation behavior during prey capture as do bats(Griffin 1958); search, approach and buzz. A similar pattern has been describedearlier for bottlenose dolphins (Evans and Powell 1967, Johnson 1967, Morozovet al. 1972). During the terminal part of the approach the click interval andclick intensity continually decreases and ends in a “buzz.” At this time the preyis 2–4 m from the porpoise or it would take the porpoise about 1 s to reach the

3Personal communication from Janni Damsgaard-Hansen, Fjørd&Bælt, Margrethes Plads 1, 5300Kerteminde, Denmark, 20 January 2011.


prey based on results from experiments with captive harbor porpoises (Verfußet al. 2009). We record similar acoustic behaviors from our tagged wild harborporpoises where a reduction in click interval to less than 10 ms can happen inabout 0.5 s (Fig. 7). Prey detection occurs earlier as indicated from captive har-bor porpoises (Verfuß et al. 2009). The terminal buzz could not be recorded fromour tagged wild harbor porpoises since the source level of the individual clickspresumably fell below the trigger level of the A-tag. Porpoise #3 showed themost intense foraging activity (Table 2), based on sequences with suddendecreasing click intervals (see Fig. 7B). We assume these sequences ended inprey capture or attempted capture. Porpoises #2 and #3 probably did some ofthe foraging at the sea bottom (Fig. 5, Table 2), a behavior others have alsoreported (see Santos and Pierce 2003). However, there was variation in the pre-sumed foraging activity among animals with most activity within the surfacelayer (0–2 m) and the bottom of the dive (Table 2). Obviously we do not knowthe species of fish our tagged porpoises were taking, but two species that harborporpoises feed on in Danish inner waters are herring (Clupea harengus) and whit-ing (Merlangius merlangus), both of which spend time near the surface, especiallyat night.4 Flat fish (Pleuronectiformes) and sandeels (Ammodytes sp.) are common onthe bottom at night.The number of foraging events resulting in prey capture cannot be stated since

some may have been unsuccessful or the characteristic click pattern may havebeen used in a different context. The low rate of possible foraging for porpoise#2 is probably due to the 142 dB threshold of the A-tag since the porpoisecould have been using low intensity signals in the shallow coastal waters whereit spent all of the time it was tagged.Harbor porpoises feed on a large variety of fish species (Santos et al. 2004) that

live within the water column as well as near and on the seafloor. Therefore it isnot surprising that we found possible foraging events in all dive phases for thethree animals. This supports the conclusion that harbor porpoises are highlyadaptive and opportunistic in their foraging ecology.Click intervals in captive animals during the search phase are between 50 and

60 ms (Verfuß et al. 2009). One might expect wild harbor porpoises to uselonger and more variable click intervals when scanning an unknown, open envi-ronment. However, our results show that click intervals in the search phase oftagged animals were from 30 to 150 ms (see Fig. 7 as an example). Captive por-poises use landmarks as orientation points (Verfuß et al. 2005). The distance to alandmark can be calculated from the time interval between searching clicks andthe estimated “lag time” (Thomas and Turl 1990, Au 1993). According toVerfuß et al. (2005) lag time ranges between 14 and 36 ms in captive harborporpoises depending on the difficulty of the task. Thus, the click interval minusthe minimum lag time divided by two and multiplied with the speed of soundin water (1.5 m/ms) gives the scanning distance. The maximum scanning dis-tances are between 12 m and 102 m for click intervals of the two possible feed-ing events shown in Figure 7, or about the same distances as for captiveporpoises in Kerteminde. If these values hold in general then harbor porpoisesare not long distance hunters.

4Personal communication from Finn Larsen, DTU Aqua, Danmarks Tekniske Universitet Char-lottenlund Slot, Jægersborg Allé 1, 2920 Charlottenlund, Denmark, 12 December 2011.


Conclusions

This study demonstrates that recording bioacoustics and dive activity com-bined with satellite-transmitted positions is possible over several days whileproviding considerable insight into the behavior of free ranging harbor por-poises. Large variability was observed among the three porpoises with echoloca-tion activity varying from 50,000 clicks per hour and the divefrequency from 6 to 179 dives per hour down to a maximum of 34 m for upto 213 s. This variation can be attributed to individual behavior, depth, typeof habitat and the prey species available. For the porpoise (#2) that stayed inthe same habitat throughout the deployment, the behavior was linked to theenvironment as shown by a consistent diurnal variation in echolocation anddiving. Such behavior can be expected in a uniform habitat where porpoisesspecialize on certain prey species. On the other hand, the ever changing physi-cal and biological environment in the waters connecting the Baltic Sea andNorth Sea requires a high level of behavioral adaptability to be able to survive,which is probably the main explanation for the behavioral variations we foundfor porpoises moving to other habitat types. However, to be able to differenti-ate between individual behavior and behavior determined by the characteristicsof a particular habitat, data from several animals exploiting the same habitatare required.In future studies it is recommended to take advantage of the rapid technological

advances in miniaturizing devices like video for monitoring hunting behavior andprey species, on-board GPS for more frequent and accurate positioning, accelerom-eters, swim speed and compasses to monitor movements in three dimensions.When these advances are combined with acoustic tags we will be able to give acontext related description of the bioacoustics and behavior of free-rangingporpoises as has been done, to some extent, for larger cetaceans in recent years.

Acknowledgments

The Danish pound net fishermen that collaborated on this project are greatly acknowl-edged. Without their help the study would not have been possible. Also the volunteersthat helped during tagging and retrieval of the tags are greatly acknowledged. We thankthe Danish Forest and Nature Agency, the Danish Research Council for Natural Sciences,the Danish National Research Foundation, the Carlsberg Fund, the University of Kiel,Research and Technology Centre (FTZ), and Research and Development Program forNew Bio-industry Initiatives in Japan for financial support. We thank P. Nachtigall, M.Wahlberg, and P. T. Madsen for discussions and comments on the manuscript. Weappreciated comments from referees that helped improve the manuscript. This study wasconducted under permissions from the Danish Forest and Nature Agency (no. SN 343/SN-0008) and the Ministry of Justice (no.1995-101-62).

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Received: 27 July 2011Accepted: 9 May 2012


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